Keeping it in the family: diverse histone recognition by conserved structural folds

References

• Adams-Cioaba MA and Min J. 2009. Structure and function of histone methylation binding proteins. Biochem Cell Biol 87:93–105.
   PubMed Web of Science ®Google Scholar
• Akhtar A, Zink D and Becker PB. 2000. Chromodomains are protein–RNA interaction modules. Nature 407:405–409.
   PubMed Web of Science ®Google Scholar
• Arita K, Ariyoshi M, Tochio H, Nakamura Y and Shirakawa M. 2008. Recognition of hemi-methylated DNA by the SRA protein UHRF1 by a base-flipping mechanism. Nature 455:818–821.
   PubMed Web of Science ®Google Scholar
• Avvakumov GV, Walker JR, Xue S, Li Y, Duan S, Bronner C, Arrowsmith CH and Dhe-Paganon S. 2008. Structural basis for recognition of hemi-methylated DNA by the SRA domain of human UHRF1. Nature 455:822–825.
   PubMedGoogle Scholar
• Ball LJ, Murzina NV, Broadhurst RW, Raine AR, Archer SJ, Stott FJ, Murzin AG, Singh PB, Domaille PJ and Laue ED. 1997. Structure of the chromatin binding (chromo) domain from mouse modifier protein 1. EMBO J 16:2473–2481.
   PubMed Web of Science ®Google Scholar
• Bedford MT. 2007. Arginine methylation at a glance. J Cell Sci 120:4243–4246.
   PubMed Web of Science ®Google Scholar
• Berger SL. 2007. The complex language of chromatin regulation during transcription. Nature 447:407–412.
   PubMed Web of Science ®Google Scholar
• Bernstein E, Duncan EM, Masui O, Gil J, Heard E and Allis CD. 2006. Mouse polycomb proteins bind differentially to methylated histone H3 and RNA and are enriched in facultative heterochromatin. Mol Cell Biol 26:2560–2569.
   PubMed Web of Science ®Google Scholar
• Bostick M, Kim JK, Esteve PO, Clark A, Pradhan S and Jacobsen SE. 2007. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 317:1760–1764.
   PubMed Web of Science ®Google Scholar
• Bottomley MJ, Stier G, Pennacchini D, Legube G, Simon B, Akhtar A, Sattler M and Musco G. 2005. NMR structure of the first PHD finger of autoimmune regulator protein (AIRE1). Insights into autoimmune polyendocrinopathy-candidiasis-ectodermal dystrophy (APECED) disease. J Biol Chem 280:11505–11512.
   PubMed Web of Science ®Google Scholar
• Botuyan MV, Lee J, Ward IM, Kim JE, Thompson JR, Chen J and Mer G. 2006. Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 127:1361–1373.
   PubMed Web of Science ®Google Scholar
• Brasher SV, Smith BO, Fogh RH, Nietlispach D, Thiru A, Nielsen PR, Broadhurst RW, Ball LJ, Murzina NV and Laue ED. 2000. The structure of mouse HP1 suggests a unique mode of single peptide recognition by the shadow chromo domain dimer. EMBO J 19:1587–1597.
   PubMed Web of Science ®Google Scholar
• Capili AD, Schultz DC, Rauscher IF and Borden KL. 2001. Solution structure of the PHD domain from the KAP-1 corepressor: structural determinants for PHD, RING and LIM zinc-binding domains. EMBO J 20:165–177.
   PubMed Web of Science ®Google Scholar
• Chakravarty S, Zeng L and Zhou MM. 2009. Structure and site-specific recognition of histone H3 by the PHD finger of human autoimmune regulator. Structure 17:670–679.
   Google Scholar
• Champagne KS, Saksouk N, Pena PV, Johnson K, Ullah M, Yang XJ, Cote J and Kutateladze TG. 2008. The crystal structure of the ING5 PHD finger in complex with an H3K4me3 histone peptide. Proteins 72:1371–1376.
   PubMed Web of Science ®Google Scholar
• Charier G, Couprie J, Alpha-Bazin B, Meyer V, Quemeneur E, Guerois R, Callebaut I, Gilquin B and Zinn-Justin S. 2004. The Tudor tandem of 53BP1: a new structural motif involved in DNA and RG-rich peptide binding. Structure 12:1551–1562.
   PubMed Web of Science ®Google Scholar
• Charlop-Powers Z, Zeng L, Zhang Q and Zhou MM. 2010. Structural insights into selective histone H3 recognition by the human Polybromo bromodomain 2. Cell Res 20:529–538.
   PubMed Web of Science ®Google Scholar
• Chen C, Jin J, James DA, Adams-Cioaba MA, Park JG, Guo Y, Tenaglia E, Xu C, Gish G, Min J and Pawson T. 2009. Mouse Piwi interactome identifies binding mechanism of Tdrkh Tudor domain to arginine methylated Miwi. Proc Natl Acad Sci USA 106:20336–20341.
   PubMed Web of Science ®Google Scholar
• Cheng D, Cote J, Shaaban S and Bedford MT. 2007. The arginine methyltransferase CARM1 regulates the coupling of transcription and mRNA processing. Mol Cell 25:71–83.
   PubMed Web of Science ®Google Scholar
• Chignola F, Gaetani M, Rebane A, Org T, Mollica L, Zucchelli C, Spitaleri A, Mannella V, Peterson P and Musco G. 2009. The solution structure of the first PHD finger of autoimmune regulator in complex with non-modified histone H3 tail reveals the antagonistic role of H3R2 methylation. Nucleic Acids Res 37:2951–2961.
   PubMed Web of Science ®Google Scholar
• Citterio E, Papait R, Nicassio F, Vecchi M, Gomiero P, Mantovani R, Di Fiore PP and Bonapace IM. 2004. Np95 is a histone-binding protein endowed with ubiquitin ligase activity. Mol Cell Biol 24:2526–2535.
   PubMed Web of Science ®Google Scholar
• Cote J and Richard S. 2005. Tudor domains bind symmetrical dimethylated arginines. J Biol Chem 280:28476–28483.
   PubMed Web of Science ®Google Scholar
• Couture JF, Collazo E and Trievel RC. 2006. Molecular recognition of histone H3 by the WD40 protein WDR5. Nat Struct Mol Biol 13:698–703.
   PubMed Web of Science ®Google Scholar
• Cowieson NP, Partridge JF, Allshire RC and McLaughlin PJ. 2000. Dimerisation of a chromo shadow domain and distinctions from the chromodomain as revealed by structural analysis. Curr Biol 10:517–525.
   PubMed Web of Science ®Google Scholar
• Dawson MA, Bannister AJ, Gottgens B, Foster SD, Bartke T, Gree AR and Kouzarides T. 2009. JAK2 phosphorylates histone H3Y41 and excludes HP1alpha from chromatin. Nature 461:819–822.
   PubMed Web of Science ®Google Scholar
• Dhalluin C, Carlson JE, Zeng L, He C, Aggarwal AK and Zhou MM. 1999. Structure and ligand of a histone acetyltransferase bromodomain. Nature 399:491–496.
   PubMed Web of Science ®Google Scholar
• Dou Y, Milne TA, Tackett AJ, Smith ER, Fukuda A, Wysocka J, Allis CD, Chait BT, Hess JL and Roeder RG. 2005. Physical association and coordinate function of the H3 K4 methyltransferase MLL1 and the H4 K16 acetyltransferase MOF. Cell 121:873–885.
   PubMed Web of Science ®Google Scholar
• Elkin SK, Ivanov D, Ewalt M, Ferguson CG, Hyberts SG, Sun ZY, Prestwich GD, Yuan J, Wagner G, Oettinger MA and Gozani OP. 2005. A PHD finger motif in the C terminus of RAG2 modulates recombination activity. J Biol Chem 280:28701–28710.
   PubMed Web of Science ®Google Scholar
• Eryilmaz J, Pan P, Amaya MF, Allali-Hassani A, Dong A, Adams-Cioaba MA, Mackenzie F, Vedadi M and Min J. 2009. Structural studies of a four-MBT repeat protein MBTD1. PLoS One 4:e7274.
   PubMed Web of Science ®Google Scholar
• Fiedler M, Sanchez-Barrena MJ, Nekrasov M, Mieszczanek J, Rybin V, Muller J, Evans P and Bienz M. 2008. Decoding of methylated histone H3 tail by the Pygo-BCL9 Wnt signaling complex. Mol Cell 30:507–518.
   PubMedGoogle Scholar
• Fischle W, Wang Y and Allis CD. 2003a. Binary switches and modification cassettes in histone biology and beyond. Nature 425:475–479.
   PubMed Web of Science ®Google Scholar
• Fischle W, Wang Y, Jacobs SA, Kim Y, Allis CD and Khorasanizadeh S. 2003b. Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev 17:1870–1881.
   PubMed Web of Science ®Google Scholar
• Flanagan JF, Mi LZ, Chruszcz M, Cymborowski M, Clines KL, Kim Y, Minor W, Rastinejad F and Khorasanizadeh S. 2005. Double chromodomains cooperate to recognize the methylated histone H3 tail. Nature 438:1181–1185.
   PubMed Web of Science ®Google Scholar
• Flanagan JF, Blus BJ, Kim D, Clines KL, Rastinejad F and Khorasanizadeh S. 2007. Molecular implications of evolutionary differences in CHD double chromodomains. J Mol Biol 369:334–342.
   PubMed Web of Science ®Google Scholar
• Friberg A, Corsini L, Mourao A and Sattler M. 2009. Structure and ligand binding of the extended Tudor domain of D. melanogaster Tudor-SN. J Mol Biol 387:921–934.
   PubMed Web of Science ®Google Scholar
• Ge YZ, Pu MT, Gowher H, Wu HP, Ding JP, Jeltsch A and Xu GL. 2004. Chromatin targeting of de novo DNA methyltransferases by the PWWP domain. J Biol Chem 279:25447–25454.
   PubMedGoogle Scholar
• Grimm C, de Ayala Alonso AG, Rybin V, Steuerwald U, Ly-Hartig N, Fischle W, Muller J and Muller CW. 2007. Structural and functional analyses of methyl-lysine binding by the malignant brain tumour repeat protein Sex comb on midleg. EMBO Rep 8:1031–1037.
   PubMedGoogle Scholar
• Grimm C, Matos R, Ly-Hartig N, Steuerwald U, Lindner D, Rybin V, Muller J and Muller CW. 2009. Molecular recognition of histone lysine methylation by the Polycomb group repressor dSfmbt. EMBO J 28:1965–1977.
   PubMedGoogle Scholar
• Guccione E, Bassi C, Casadio F, Martinato F, Cesaroni M, Schuchlautz H, Luscher B and Amati B. 2007. Methylation of histone H3R2 by PRMT6 and H3K4 by an MLL complex are mutually exclusive. Nature 449:933–937.
   PubMed Web of Science ®Google Scholar
• Guo Y, Nady N, Qi C, Allali-Hassani A, Zhu H, Pan P, Adams-Cioaba MA, Amaya MF, Dong A, Vedadi M, Schapira M, Read RJ, Arrowsmith CH and Min J. 2009. Methylation-state-specific recognition of histones by the MBT repeat protein L3MBTL2. Nucleic Acids Res 37:2204–2210.
   Google Scholar
• Han Z, Guo L, Wang H, Shen Y, Deng XW and Chai J. 2006. Structural basis for the specific recognition of methylated histone H3 lysine 4 by the WD-40 protein WDR5. Mol Cell 22:137–144.
   PubMed Web of Science ®Google Scholar
• Hashimoto H, Horton JR, Zhang X, Bostick M, Jacobsen SE and Cheng X. 2008. The SRA domain of UHRF1 flips 5-methylcytosine out of the DNA helix. Nature 455:826–829.
   PubMedGoogle Scholar
• Huang Y, Fang J, Bedford MT, Zhang Y and Xu RM. 2006a. Recognition of histone H3 lysine-4 methylation by the double tudor domain of JMJD2A. Science 312:748–751.
   PubMed Web of Science ®Google Scholar
• Huang Y, Myers MP and Xu RM. 2006b. Crystal structure of the HP1-EMSY complex reveals an unusual mode of HP1 binding. Structure 14:703–712.
   PubMed Web of Science ®Google Scholar
• Hudson BP, Martinez-Yamout MA, Dyson HJ and Wright PE. 2000. Solution structure and acetyl-lysine binding activity of the GCN5 bromodomain. J Mol Biol 304:355–370.
   PubMed Web of Science ®Google Scholar
• Hughes RM, Wiggins KR, Khorasanizadeh S and Waters ML. 2007. Recognition of trimethyllysine by a chromodomain is not driven by the hydrophobic effect. Proc Natl Acad Sci USA 104:11184–11188.
   PubMed Web of Science ®Google Scholar
• Hung T, Binda O, Champagne KS, Kuo AJ, Johnson K, Chang HY, Simon MD, Kutateladze TG and Gozani O. 2009. ING4 mediates crosstalk between histone H3 K4 trimethylation and H3 acetylation to attenuate cellular transformation. Mol Cell 33:248–256.
   PubMed Web of Science ®Google Scholar
• Huyen Y, Zgheib O, Ditullio RA, Jr., Gorgoulis VG, Zacharatos P, Petty TJ, Sheston EA, Mellert HS, Stavridi ES and Halazonetis TD. 2004. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432:406–411.
   PubMed Web of Science ®Google Scholar
• Ivanov AV, Peng H, Yurchenko V, Yap KL, Negorev DG, Schultz DC, Psulkowski E, Fredericks WJ, White DE, Maul GG, Sadofsky MJ, Zhou M-M,and Rauscher FJ. 2007. PHD domain-mediated E3 ligase activity directs intramolecular sumoylation of an adjacent bromodomain required for gene silencing. Mol Cell 28:823–837.
   PubMed Web of Science ®Google Scholar
• Jacobs SA and Khorasanizadeh S. 2002. Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail. Science 295:2080–2083.
   PubMed Web of Science ®Google Scholar
• Jacobson RH, Ladurner AG, King DS and Tjian R. 2000. Structure and function of a human TAFII250 double bromodomain module. Science 288:1422–1425.
   PubMed Web of Science ®Google Scholar
• Jaenisch R and Bird A. 2003. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33 Suppl:245–254.
   PubMed Web of Science ®Google Scholar
• Jin J, Xie X, Chen C, Park JG, Stark C, James DA, Olhovsky M, Linding R, Mao Y and Pawson T. 2009. Eukaryotic protein domains as functional units of cellular evolution. Sci Signal 2:ra76.
   PubMed Web of Science ®Google Scholar
• Kang X, Qi Y, Zuo Y, Wang Q, Zou Y, Schwartz RJ, Cheng J and Yeh ET. 2010. SUMO-specific protease 2 is essential for suppression of polycomb group protein-mediated gene silencing during embryonic development. Mol Cell 38:191–201.
   PubMed Web of Science ®Google Scholar
• Karagianni P, Amazit L, Qin J and Wong J. 2008. ICBP90, a novel methyl K9 H3 binding protein linking protein ubiquitination with heterochromatin formation. Mol Cell Biol 28:705–717.
   PubMedGoogle Scholar
• Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Rivea Morales D, Thomas K, Presser A, Bernstein BE, van Oudenaarden A, Regev A, Lander ES and Rinn JL. 2009. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci USA 106:11667–11672.
   PubMed Web of Science ®Google Scholar
• Kim D, Blus BJ, Chandra V, Huang P, Rastinejad F and Khorasanizadeh S. 2010. Corecognition of DNA and a methylated histone tail by the MSL3 chromodomain. Nat Struct Mol Biol 17:1027–1029.
   PubMedGoogle Scholar
• Kim J, Daniel J, Espejo A, Lake A, Krishna M, Xia L, Zhang Y and Bedford MT. 2006. Tudor, MBT and chromo domains gauge the degree of lysine methylation. EMBO Rep 7:397–403.
   PubMed Web of Science ®Google Scholar
• Kirmizis A, Santos-Rosa H, Penkett CJ, Singer MA, Vermeulen M, Mann M, Bähler J, Green RD and Kouzarides T. 2007. Arginine methylation at histone H3R2 controls deposition of H3K4 trimethylation. Nature 449:928–932.
   PubMed Web of Science ®Google Scholar
• Kirmizis A, Santos-Rosa H, Penkett CJ, Singer MA, Green RD and Kouzarides T. 2009. Distinct transcriptional outputs associated with mono- and dimethylated histone H3 arginine 2. Nat Struct Mol Biol 16:449–451.
   PubMed Web of Science ®Google Scholar
• Kouzarides T. 2007. Chromatin modifications and their function. Cell 128:693–705.
   PubMed Web of Science ®Google Scholar
• Kwan AH, Gell DA, Verger A, Crossley M, Matthews JM and Mackay JP. 2003. Engineering a protein scaffold from a PHD finger. Structure 11:803–813.
   PubMed Web of Science ®Google Scholar
• Lan F, Collins RE, De Cegli R, Alpatov R, Horton JR, Shi X, Gozani O, Cheng X and Shi Y. 2007. Recognition of unmethylated histone H3 lysine 4 links BHC80 to LSD1-mediated gene repression. Nature 448:718–722.
   PubMed Web of Science ®Google Scholar
• Lange M, Kaynak B, Forster UB, Tonjes M, Fischer JJ, Grimm C, Schlesinger J, Just S, Dunkel I, Krueger T, Mebus S, Lehrach H, Lurz R, Gobom J, Rottbauer W, Abdelilah-Seyfried S and Sperling S. 2008. Regulation of muscle development by DPF3, a novel histone acetylation and methylation reader of the BAF chromatin remodeling complex. Genes Dev 22:2370–2384.
   PubMed Web of Science ®Google Scholar
• Laue K, Daujat S, Crump JG, Plaster N, Roehl HH, Kimmel CB, Schneider R and Hammerschmidt M. 2008. The multidomain protein Brpf1 binds histones and is required for Hox gene expression and segmental identity. Development 135:1935–1946.
   PubMedGoogle Scholar
• Lee J, Thompson JR, Botuyan MV and Mer G. 2008. Distinct binding modes specify the recognition of methylated histones H3K4 and H4K20 by JMJD2A-tudor. Nat Struct Mol Biol 15:109–111.
   PubMed Web of Science ®Google Scholar
• Lee MS, Edwards RA, Thede GL and Glover JN. 2005. Structure of the BRCT repeat domain of MDC1 and its specificity for the free COOH-terminal end of the gamma-H2AX histone tail. J Biol Chem 280:32053–32056.
   PubMed Web of Science ®Google Scholar
• Li H, Ilin S, Wang W, Duncan EM, Wysocka J, Allis CD and Patel DJ. 2006. Molecular basis for site-specific read-out of histone H3K4me3 by the BPTF PHD finger of NURF. Nature 442:91–95.
   PubMed Web of Science ®Google Scholar
• Li H, Fischle W, Wang W, Duncan EM, Liang L, Murakami-Ishibe S, Allis CD and Patel DJ. 2007. Structural basis for lower lysine methylation state-specific readout by MBT repeats of L3MBTL1 and an engineered PHD finger. Mol Cell 28:677–691.
   PubMedGoogle Scholar
• Lukasik SM, Cierpicki T, Borloz M, Grembecka J, Everett A and Bushweller JH. 2006. High resolution structure of the HDGF PWWP domain: a potential DNA binding domain. Protein Sci 15:314–323.
   PubMed Web of Science ®Google Scholar
• Macdonald N, Welburn JP, Noble ME, Nguyen A, Yaffe MB, Clynes D, Moggs JG, Orphanides G, Thomson S, Edmunds JW, Clayton AL, Endicott JA and Mahadevan LC. 2005. Molecular basis for the recognition of phosphorylated and phosphoacetylated histone h3 by 14-3-3. Mol Cell 20:199–211.
   PubMed Web of Science ®Google Scholar
• Margueron R, Justin N, Ohno K, Sharpe ML, Son J, Drury WJ 3rd, Voigt P, Martin SR, Taylor WR, De Marco V, Pirrotta V, Reinberg D and Gamblin SJ. 2009. Role of the polycomb protein EED in the propagation of repressive histone marks. Nature 461:762–767.
   PubMed Web of Science ®Google Scholar
• Maurer-Stroh S, Dickens NJ, Hughes-Davies L, Kouzarides T, Eisenhaber F and Ponting CP. 2003. The Tudor domain ‘Royal Family’: Tudor, plant Agenet, Chromo, PWWP and MBT domains. Trends Biochem Sci 28:69–74.
   PubMed Web of Science ®Google Scholar
• Min J, Zhang Y, and Xu R-M. 2003. Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Genes Dev 17:1823–1828.
   PubMedGoogle Scholar
• Min J, Allali-Hassani A, Nady N, Qi C, Ouyang H, Liu Y, MacKenzie F, Vedadi M and Arrowsmith CH. 2007. L3MBTL1 recognition of mono- and dimethylated histones. Nat Struct Mol Biol 14:1229–1230.
   PubMed Web of Science ®Google Scholar
• Moriniere J, Rousseaux S, Steuerwald U, Soler-Lopez M, Curtet S, Vitte AL, Govin J, Gaucher J, Sadoul K, Hart DJ, Krijgsveld J, Khochbin S, Muller CW and Petosa C. 2009. Cooperative binding of two acetylation marks on a histone tail by a single bromodomain. Nature 461:664–668.
   PubMed Web of Science ®Google Scholar
• Mujtaba S, He Y, Zeng L, Farooq A, Carlson JE, Ott M, Verdin E and Zhou MM. 2002. Structural basis of lysine-acetylated HIV-1 Tat recognition by PCAF bromodomain. Mol Cell 9:575–586.
   PubMed Web of Science ®Google Scholar
• Mujtaba S, He Y, Zeng L, Yan S, Plotnikova O, Sachchidanand Sanchez R, Zeleznik-Le NJ, Ronai Z and Zhou MM. 2004. Structural mechanism of the bromodomain of the coactivator CBP in p53 transcriptional activation. Mol Cell 13:251–263.
   PubMed Web of Science ®Google Scholar
• Murzina NV, Pei XY, Zhang W, Sparkes M, Vicente-Garcia J, Pratap JV, McLaughlin SH, Ben-Shahar TR, Verreault A, Luisi BF and Laue ED. 2008. Structural basis for the recognition of histone H4 by the histone-chaperone RbAp46. Structure 16:1077–1085.
   PubMed Web of Science ®Google Scholar
• Nakamura Y, Umehara T, Nakano K, Jang MK, Shirouzu M, Morita S, Uda-Tochio H, Hamana H, Terada T, Adachi N, Matsumoto T, Tanaka A, Horikoshi M, Ozato K, Padmanabhan B and Yokoyama S. 2007. Crystal structure of the human BRD2 bromodomain: insights into dimerization and recognition of acetylated histone H4. J Biol Chem 282:4193–4201.
   PubMed Web of Science ®Google Scholar
• Nameki N, Tochio N, Koshiba S, Inoue M, Yabuki T, Aoki M, Seki E, Matsuda T, Fujikura Y, Saito M, Ikari M, Watanabe M, Terada T, Shirouzu M, Yoshida M, Hirota H, Tanaka A, Hayashizaki Y, Guntert P, Kigawa T and Yokoyama S. 2005. Solution structure of the PWWP domain of the hepatoma-derived growth factor family. Protein Sci 14:756–764.
   PubMed Web of Science ®Google Scholar
• Nielsen PR, Nietlispach D, Mott HR, Callaghan J, Bannister A, Kouzarides T, Murzin AG, Murzina NV and Laue ED. 2002. Structure of the HP1 chromodomain bound to histone H3 methylated at lysine 9. Nature 416:103–107.
   PubMed Web of Science ®Google Scholar
• Nielsen PR, Nietlispach D, Buscaino A, Warner RJ, Akhtar A, Murzin AG, Murzina NV and Laue ED. 2005. Structure of the chromo barrel domain from the MOF acetyltransferase. J Biol Chem 280:32326–32331.
   PubMedGoogle Scholar
• Okuda M, Horikoshi M and Nishimura Y. 2007. Structural polymorphism of chromodomains in Chd1. J Mol Biol 365:1047–1062.
   PubMed Web of Science ®Google Scholar
• Owen DJ, Ornaghi P, Yang JC, Lowe N, Evans PR, Ballario P, Neuhaus D, Filetici P and Travers AA. 2000. The structural basis for the recognition of acetylated histone H4 by the bromodomain of histone acetyltransferase gcn5p. EMBO J 19:6141–6149.
   PubMed Web of Science ®Google Scholar
• Palacios A, Garcia P, Padro D, Lopez-Hernandez E, Martin I and Blanco FJ. 2006. Solution structure and NMR characterization of the binding to methylated histone tails of the plant homeodomain finger of the tumour suppressor ING4. FEBS Lett 580:6903–6908.
   PubMed Web of Science ®Google Scholar
• Palacios A, Munoz IG, Pantoja-Uceda D, Marcaida MJ, Torres D, Martin-Garcia JM, Luque I, Montoya G and Blanco FJ. 2008. Molecular basis of histone H3K4me3 recognition by ING4. J Biol Chem 283:15956–15964.
   PubMed Web of Science ®Google Scholar
• Papait R, Pistore C, Grazini U, Babbio F, Cogliati S, Pecoraro D, Brino L, Morand AL, Dechampesme AM, Spada F, Leonhardt H, McBlane F, Oudet P and Bonapace IM. 2008. The PHD domain of Np95 (mUHRF1) is involved in large-scale reorganization of pericentromeric heterochromatin. Mol Biol Cell 19:3554–3563.
   PubMedGoogle Scholar
• Pascual J, Martinez-Yamout M, Dyson HJ and Wright PE. 2000. Structure of the PHD zinc finger from human Williams-Beuren syndrome transcription factor. J Mol Biol 304:723–729.
   PubMed Web of Science ®Google Scholar
• Patel A, Dharmarajan V and Cosgrove MS. 2008a. Structure of WDR5 bound to mixed lineage leukemia protein-1 peptide. J Biol Chem 283:32158–32161.
   PubMed Web of Science ®Google Scholar
• Patel A, Vought VE, Dharmarajan V and Cosgrove MS. 2008b. A conserved arginine-containing motif crucial for the assembly and enzymatic activity of the mixed lineage leukemia protein-1 core complex. J Biol Chem 283:32162–32175.
   PubMed Web of Science ®Google Scholar
• Pena PV, Davrazou F, Shi X, Walter KL, Verkhusha VV, Gozani O, Zhao R and Kutateladze TG. 2006. Molecular mechanism of histone H3K4me3 recognition by plant homeodomain of ING2. Nature 442:100–103.
   PubMed Web of Science ®Google Scholar
• Pena PV, Hom RA, Hung T, Lin H, Kuo AJ, Wong RP, Subach OM, Champagne KS, Zhao R, Verkhusha VV, Li G, Gozani O and Kutateladze TG. 2008. Histone H3K4me3 binding is required for the DNA repair and apoptotic activities of ING1 tumor suppressor. J Mol Biol 380:303–312.
   PubMed Web of Science ®Google Scholar
• Qian C, Li S, Jakoncic J, Zeng L, Walsh MJ and Zhou MM. 2008. Structure and hemimethylated CpG binding of the SRA domain from human UHRF1. J Biol Chem 283:34490–34494.
   Google Scholar
• Qiu C, Sawada K, Zhang X and Cheng X. 2002. The PWWP domain of mammalian DNA methyltransferase Dnmt3b defines a new family of DNA-binding folds. Nat Struct Biol 9:217–224.
   PubMedGoogle Scholar
• Ramon-Maiques S, Kuo AJ, Carney D, Matthews AG, Oettinger MA, Gozani O and Yang W. 2007. The plant homeodomain finger of RAG2 recognizes histone H3 methylated at both lysine-4 and arginine-2. Proc Natl Acad Sci USA 104:18993–18998.
   PubMed Web of Science ®Google Scholar
• Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E and Chang HY. 2007. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129:1311–1323.
   PubMed Web of Science ®Google Scholar
• Roy S, Musselman CA, Kachirskaia I, Hayashi R, Glass KC, Nix JC, Gozani O, Appella E and Kutateladze TG. 2010. Structural Insight into p53 Recognition by the 53BP1 Tandem Tudor Domain. J Mol Biol 398:489–496.
   PubMed Web of Science ®Google Scholar
• Ruthenburg AJ, Allis CD and Wysocka J. 2007a. Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. Mol Cell 25:15–30.
   PubMed Web of Science ®Google Scholar
• Ruthenburg AJ, Li H, Patel DJ and Allis CD. 2007b. Multivalent engagement of chromatin modifications by linked binding modules. Nat Rev Mol Cell Biol 8:983–994.
   PubMed Web of Science ®Google Scholar
• Sanchez R and Zhou MM. 2009. The role of human bromodomains in chromatin biology and gene transcription. Curr Opin Drug Discov Devel 12:659–665.
   PubMedGoogle Scholar
• Santiveri CM, Lechtenberg BC, Allen MD, Sathyamurthy A, Jaulent AM, Freund SM and Bycroft M. 2008. The malignant brain tumor repeats of human SCML2 bind to peptides containing monomethylated lysine. J Mol Biol 382:1107–1112.
   PubMedGoogle Scholar
• Sathyamurthy A, Allen MD, Murzin AG and Bycroft M. 2003. Crystal structure of the malignant brain tumor (MBT) repeats in Sex Comb on Midleg-like 2 (SCML2). J Biol Chem 278:46968–46973.
   PubMed Web of Science ®Google Scholar
• Schuetz A, Allali-Hassani A, Martin F, Loppnau P, Vedadi M, Bochkarev A, Plotnikov AN, Arrowsmith CH and Min J. 2006. Structural basis for molecular recognition and presentation of histone H3 by WDR5. EMBO J 25:4245–4252.
   PubMed Web of Science ®Google Scholar
• Schwartz YB and Pirrotta V. 2007. Polycomb silencing mechanisms and the management of genomic programmes. Nat Rev Genet 8:9–22.
   PubMed Web of Science ®Google Scholar
• Seet BT, Dikic I, Zhou MM and Pawson T. 2006. Reading protein modifications with interaction domains. Nat Rev Mol Cell Biol 7:473–483.
   PubMed Web of Science ®Google Scholar
• Selenko P, Sprangers R, Stier G, Buhler D, Fischer U and Sattler M. 2001. SMN tudor domain structure and its interaction with the Sm proteins. Nat Struct Biol 8:27–31.
   PubMedGoogle Scholar
• Sharif J, Muto M, Takebayashi S, Suetake I, Iwamatsu A, Endo TA, Shinga J, Mizutani-Koseki Y, Toyoda T, Okamura K, Tajima S, Mitsuya K, Okano M and Koseki H. 2007. The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 450:908–912.
   PubMed Web of Science ®Google Scholar
• Shen W, Xu C, Huang W, Zhang J, Carlson JE, Tu X, Wu J and Shi Y. 2007. Solution structure of human Brg1 bromodomain and its specific binding to acetylated histone tails. Biochemistry 46:2100–2110.
   PubMed Web of Science ®Google Scholar
• Shi X, Hong T, Walter KL, Ewalt M, Michishita E, Hung T, Carney D, Pena P, Lan F, Kaadige MR, Lacoste N, Cayrou C, Davrazou F, Saha A, Cairns BR, Ayer DE, Kutateladze TG, Shi Y, Cote J, Chua KF and Gozani O. 2006. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442:96–99.
   PubMed Web of Science ®Google Scholar
• Shimojo H, Sano N, Moriwaki Y, Okuda M, Horikoshi M and Nishimura Y. 2008. Novel structural and functional mode of a knot essential for RNA binding activity of the Esa1 presumed chromodomain. J Mol Biol 378:987–1001.
   PubMed Web of Science ®Google Scholar
• Sims RJ, 3rd Chen, CF, Santos-Rosa H, Kouzarides T, Patel SS and Reinberg D. 2005. Human but not yeast CHD1 binds directly and selectively to histone H3 methylated at lysine 4 via its tandem chromodomains. J Biol Chem 280:41789–41792.
   PubMed Web of Science ®Google Scholar
• Singh M, Popowicz GM, Krajewski M and Holak TA. 2007. Structural ramification for acetyl-lysine recognition by the bromodomain of human BRG1 protein, a central ATPase of the SWI/SNF remodeling complex. Chembiochem 8:1308–1316.
   PubMed Web of Science ®Google Scholar
• Slater LM, Allen MD and Bycroft M. 2003. Structural variation in PWWP domains. J Mol Biol 330:571–576.
   PubMed Web of Science ®Google Scholar
• Song JJ and Kingston RE. 2008. WDR5 interacts with mixed lineage leukemia (MLL) protein via the histone H3-binding pocket. J Biol Chem 283:35258–35264.
   PubMed Web of Science ®Google Scholar
• Song JJ, Garlick JD and Kingston RE. 2008. Structural basis of histone H4 recognition by p55. Genes Dev 22:1313–1318.
   PubMed Web of Science ®Google Scholar
• Southall SM, Wong PS, Odho Z, Roe SM and Wilson JR. 2009. Structural basis for the requirement of additional factors for MLL1 SET domain activity and recognition of epigenetic marks. Mol Cell 33:181–191.
   PubMed Web of Science ®Google Scholar
• Sprangers R, Groves MR, Sinning I and Sattler M. 2003. High-resolution X-ray and NMR structures of the SMN Tudor domain: conformational variation in the binding site for symmetrically dimethylated arginine residues. J Mol Biol 327:507–520.
   PubMed Web of Science ®Google Scholar
• Strahl BD and Allis CD. 2000. The language of covalent histone modifications. Nature 403:41–45.
   PubMed Web of Science ®Google Scholar
• Stucki M, Clapperton JA, Mohammad D, Yaffe MB, Smerdon SJ and Jackson SP. 2005. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123:1213–1226.
   PubMed Web of Science ®Google Scholar
• Sue SC, Lee WT, Tien SC, Lee SC, Yu JG, Wu WJ, Wu WG and Huang TH. 2007. PWWP module of human hepatoma-derived growth factor forms a domain-swapped dimer with much higher affinity for heparin. J Mol Biol 367:456–472.
   PubMed Web of Science ®Google Scholar
• Suganuma T and Workman JL. 2008. Crosstalk among histone modifications. Cell 135:604–607.
   PubMed Web of Science ®Google Scholar
• Sun B, Hong J, Zhang P, Dong X, Shen X, Lin D and Ding J. 2008. Molecular basis of the interaction of Saccharomyces cerevisiae Eaf3 chromo domain with methylated H3K36. J Biol Chem 283:36504–36512.
   PubMed Web of Science ®Google Scholar
• Sun H, Liu J, Zhang J, Shen W, Huang H, Xu C, Dai H, Wu J and Shi Y. 2007. Solution structure of BRD7 bromodomain and its interaction with acetylated peptides from histone H3 and H4. Biochem Biophys Res Commun 358:435–441.
   PubMed Web of Science ®Google Scholar
• Taverna SD, Ilin S, Rogers RS, Tanny JC, Lavender H, Li H, Baker L, Boyle J, Blair LP, Chait BT, Patel DJ, Aitchison JD, Tackett AJ and Allis CD. 2006. Yng1 PHD finger binding to H3 trimethylated at K4 promotes NuA3 HAT activity at K14 of H3 and transcription at a subset of targeted ORFs. Mol Cell 24:785–796.
   PubMed Web of Science ®Google Scholar
• Taverna SD, Li H, Ruthenburg AJ, Allis CD and Patel DJ. 2007. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat Struct Mol Biol 14:1025–1040.
   PubMed Web of Science ®Google Scholar
• Thiru A, Nietlispach D, Mott HR, Okuwaki M, Lyon D, Nielsen PR, Hirshberg M, Verreault A, Murzina NV and Laue ED. 2004. Structural basis of HP1/PXVXL motif peptide interactions and HP1 localisation to heterochromatin. EMBO J 23:489–499.
   PubMed Web of Science ®Google Scholar
• Thompson M. 2009. Polybromo-1: the chromatin targeting subunit of the PBAF complex. Biochimie 91:309–319.
   PubMed Web of Science ®Google Scholar
• Trievel RC and Shilatifard A. 2009. WDR5, a complexed protein. Nat Struct Mol Biol 16:678–680.
   PubMed Web of Science ®Google Scholar
• Turner BM. 2002. Cellular memory and the histone code. Cell 111:285–291.
   PubMed Web of Science ®Google Scholar
• Unoki M, Nishidate T and Nakamura Y. 2004. ICBP90, an E2F-1 target, recruits HDAC1 and binds to methyl-CpG through its SRA domain. Oncogene 23:7601–7610.
   PubMed Web of Science ®Google Scholar
• VanDemark AP, Kasten MM, Ferris E, Heroux A, Hill CP and Cairns BR. 2007. Autoregulation of the rsc4 tandem bromodomain by gcn5 acetylation. Mol Cell 27:817–828.
   PubMed Web of Science ®Google Scholar
• Vezzoli A, Bonadies N, Allen MD, Freund SM, Santiveri CM, Kvinlaug BT, Huntly BJ, Gottgens B and Bycroft M. 2010. Molecular basis of histone H3K36me3 recognition by the PWWP domain of Brpf1. Nat Struct Mol Biol 17:617–619.
   PubMed Web of Science ®Google Scholar
• Vollmuth F, Blankenfeldt W and Geyer M. 2009. Structures of the dual bromodomains of the P-TEFb-activating protein Brd4 at atomic resolution. J Biol Chem 284:36547–36556.
   PubMed Web of Science ®Google Scholar
• Wang GG, Song J, Wang Z, Dormann HL, Casadio F, Li H, Luo JL, Patel DJ and Allis CD. 2009. Haematopoietic malignancies caused by dysregulation of a chromatin-binding PHD finger. Nature 459:847–851.
   PubMed Web of Science ®Google Scholar
• Wang WK, Tereshko V, Boccuni P, MacGrogan D, Nimer SD and Patel DJ. 2003. Malignant brain tumor repeats: a three-leaved propeller architecture with ligand/peptide binding pockets. Structure 11:775–789.
   PubMed Web of Science ®Google Scholar
• Wang Y, Reddy B, Thompson J, Wang H, Noma K, Yates JR, 3rd, and Jia S. 2009b. Regulation of Set9-mediated H4K20 methylation by a PWWP domain protein. Mol Cell 33:428–437.
   PubMed Web of Science ®Google Scholar
• Wen H, Li J, Song T, Lu M, Kan PY, Lee MG, Sha B and Shi X. 2010. Recognition of histone H3K4 trimethylation by the plant homeodomain of PHF2 modulates histone demethylation. J Biol Chem 285:9322–9326.
   PubMed Web of Science ®Google Scholar
• Wysocka J, Swigut T, Milne TA, Dou Y, Zhang X, Burlingame AL, Roeder RG, Brivanlou AH and Allis CD. 2005. WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell 121:859–872.
   PubMed Web of Science ®Google Scholar
• Wysocka J, Swigut T, Xiao H, Milne TA, Kwon SY, Landry J, Kauer M, Tackett AJ, Chait BT, Badenhorst P, Wu C and Allis CD. 2006. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 442:86–90.
   PubMed Web of Science ®Google Scholar
• Xu C, Cui G, Botuyan MV and Mer G. 2008. Structural basis for the recognition of methylated histone H3K36 by the Eaf3 subunit of histone deacetylase complex Rpd3S. Structure 16:1740–1750.
   PubMed Web of Science ®Google Scholar
• Yap KL, Li S, Munoz-Cabello AM, Raguz S, Zeng L, Mujtaba S, Gil J, Walsh MJ and Zhou MM. 2010. Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol Cell 38:662–674.
   PubMed Web of Science ®Google Scholar
• Yap KL, and Zhou M-M. 2006. Structure and function of protein modules in chromatin biology. Results Probl Cell Differ 41:1–23.
   PubMedGoogle Scholar
• Zeng L, Yap KL, Ivanov AV, Wang X, Mujtaba S, Plotnikova O, Rauscher FJ, 3rd,and Zhou MM. 2008a. Structural insights into human KAP1 PHD finger-bromodomain and its role in gene silencing. Nat Struct Mol Biol 15:626–633.
   PubMed Web of Science ®Google Scholar
• Zeng L, Zhang Q, Gerona-Navarro G, Moshkina N and Zhou MM. 2008b. Structural basis of site-specific histone recognition by the bromodomains of human coactivators PCAF and CBP/p300. Structure 16:643–652.
   PubMed Web of Science ®Google Scholar
• Zeng L, Zhang Q, Li S, Plotnikov AN, Walsh MJ and Zhou MM. 2010. Mechanism and regulation of acetylated histone binding by the tandem PHD finger of DPF3b. Nature 466:258–262.
   PubMed Web of Science ®Google Scholar
• Zhang P, Du J, Sun B, Dong X, Xu G, Zhou J, Huang Q, Liu Q, Hao Q and Ding J. 2006. Structure of human MRG15 chromo domain and its binding to Lys36-methylated histone H3. Nucleic Acids Res 34:6621–6628.
   PubMedGoogle Scholar
• Zhang Q, Chakravarty S, Ghersi D, Zeng L, Plotnikov AN, Sanchez R and Zhou MM. 2010. Biochemical profiling of histone binding selectivity of the yeast bromodomain family. PLoS One 5:e8903.
   Web of Science ®Google Scholar
• Zhao Q, Qin L, Jiang F, Wu B, Yue W, Xu F, Rong Z, Yuan H, Xie X, Gao Y, Bai C, Bartlam M, Pei X and Rao Z. 2007. Structure of human spindlin1. Tandem tudor-like domains for cell cycle regulation. J Biol Chem 282:647–656.
   PubMed Web of Science ®Google Scholar